Diversity, Distribution, Systematics and Conservation Status of Podocarpaceae

Among conifer families, Podocarpaceae is the second largest, with amazing diversity and functional traits, and it is the dominant Southern Hemisphere conifer family. However, comprehensive studies on diversity, distribution, systematic and ecophysiological aspects of the Podocarpaceae are sparse. We aim to outline and evaluate the current and past diversity, distribution, systematics, ecophysiological adaptations, endemism, and conservation status of podocarps. We analyzed data on the diversity and distribution of living and extinct macrofossil taxa and combined it with genetic data to reconstruct an updated phylogeny and understand historical biogeography. Podocarpaceae today contains 20 genera and approximately 219 taxa (201 species, 2 subspecies, 14 varieties and 2 hybrids) placed in three clades, plus a paraphyletic group/grade of four distinct genera. Macrofossil records show the presence of more than 100 podocarp taxa globally, dominantly from the Eocene–Miocene. Australasia (New Caledonia, Tasmania, New Zealand, and Malesia) is the hotspot of living podocarps diversity. Podocarps also show remarkable adaptations from broad to scale leaves, fleshy seed cones, animal dispersal, shrubs to large trees, from lowland to alpine regions and rheophyte to a parasite (including the only parasitic gymnosperm—Parasitaxus) and a complex pattern of seed and leaf functional trait evolution.


Introduction
Conifers are economically and ecologically important, form extensive forests in both Hemispheres and are currently the most diverse gymnosperms. There are seven conifer families (Araucariaceae, Cupressaceae, Pinaceae, Podocarpaceae, Sciadopityaceae, Cephalotaxaceae and Taxaceae), including 72 genera and approximately 702 species [1]. They are estimated to have evolved in the late Devonian from progymnosperms, and then dominated the Mesozoic Era [2][3][4]. Leslie et al. [5] investigated the evolutionary dynamics of conifers on a hemispheric scale based on molecular studies of 489 species and concluded that extant conifers have diverged in the Neogene with older splits in the Southern Hemisphere. Pinaceae and Cupressaceae have their main distribution in the temperate and subtropical regions of the Northern Hemisphere, while the Southern Hemisphere conifers are dominated by the Araucariaceae, Podocarpaceae and the Callitroideae of the Cupressaceae. The podocarps are monoecious and dioecious evergreen trees, shrubs, and subshrubs with mostly spirally arranged leaves and fleshy cones [6]. They are morphologically highly diverse [7,8]. Although the ecological and environmental variation (mostly rainforest and wet montane) is restricted, the morphological variation in leaves and seed cones is very high [9,10]. The extant and extinct taxa present in Australasia and South America show the wider distribution of the family across Gondwana in the past. Phylogenetically,  I. Podocarpoid clade-four genera, i.e., Afrocarpus, Nageia, Podocarpus and Retrophyllum. The suggested crown age for the Podocarpoid clade is approximately 75 Ma . The phylogeny also supports the split of Podocarpus into two subgenera i.e., Foliolatus and Podocarpus.

2.
Afrocarpus has five species distributed across Africa.

3.
Dacrycarpus has nine species and two varieties distributed in New Caledonia, New Zealand, some Pacific Islands and Southeast Asia ( Figure 3A).

4.
Dacrydium has 20 species and two hybrids distributed in New Caledonia, New Zealand, some Pacific Islands and Southeast Asia.

5.
Falcatifolium has six species distributed in New Caledonia, Papua New Guinea, Indonesia, Malaysia, the Philippines and Brunei Darussalam.
Manoao has one species distributed in New Zealand. 8.
Pherosphaera has two species endemic to Australia. 9.
Lagarostrobos has one species endemic to Australia. 10. Microcachrys has one species endemic to Australia ( Figure 3B). 11. Lepidothamnus has three species distributed in Argentina, Chile and New Zealand. 12 The Podocarpaceae has its highest diversity of genera in New Zealand (nine) with fewer in other regions New Caledonia and Malesia (eight), Australia (seven), South America (four) and Africa and Asia (two). Of the 20 genera, three are endemic to Australia and two are endemic to New Zealand. Countries with a rich diversity of podocarps include Indonesia (51 species), Papua New Guinea (43 species

Podocarpaceae in Space and Time
This checklist consists of macrofossils assigned to extant podocarp genera and includes more than one hundred taxa from the Cretaceous to the Pleistocene ( Table 2). The macrofossils are predominantly recorded from Eocene-Miocene deposits. Australian and New Zealand macrofossil records dominate. Most of the macrofossils are foliage but well-

Podocarpaceae in Space and Time
This checklist consists of macrofossils assigned to extant podocarp genera and includes more than one hundred taxa from the Cretaceous to the Pleistocene ( Table 2). The macrofossils are predominantly recorded from Eocene-Miocene deposits. Australian and New Zealand macrofossil records dominate. Most of the macrofossils are foliage but well-preserved reproductive parts (seed and pollen cones) are also recorded for Lepidothamnus, Lagarostrobos, Dacrycarpus, Phyllocladus, Podocarpus and Nageia. Extant podocarps dominate in the Southern Hemisphere and analysis of extinct taxa assigned to living podocarp genera supports their past importance in the Southern Hemisphere (Table 2). A number of extinct species assigned to Podocarpaceae genera have been reported from Australia, New Zealand and South America [26]. An analysis shows that:          [28,30,[32][33][34][35][36][37][38][39][40][41][42][43]45,71,76]. Although Dacrycarpus currently has no living species in Australia or South America, the fossil record shows its extensive distribution in both those landmasses in the past.

4.
Falcatifolium has only one fossil extinct species (F. eocenica) from the Middle Eocene of Victoria, Australia [49]. Currently, Australia has no living species of Falcatifolium.

8.
Halocarpus has a single occurrence of one extinct species (Halocarpus highstedii) reported from the Oligocene-Miocene of New Zealand [39].

9.
Manoao colensoi has a fossil record from the Oligocene of Cethana, Tasmania (Australia) (reported as Lagarostrobos colensoi) [38], showing that this current New Zealand endemic genus was once also distributed in Australia. 10. Lepidothamnus has three fossil records: L. intermedius from the Miocene in New Zealand [30], L. diemenensis from the Eocene of Hasties, Tasmania [28] and an undescribed extinct species from the middle Cretaceous of Winton, Queensland [51]. This indicates a wider distribution of Lepidothamnus in the Late Mesozoic across the Southern Gondwana regions [51]. 11. Lagarostrobos has two fossil records, e.g., L. marginatus from the Early Oligocene and the extant L. franklinii from the Early Pleistocene in Tasmania, Australia [33,34,39,45,50]. Current and macrofossil records suggest a narrow distribution and endemism to Australia for this genus. 12. Phyllocladus has seven fossil species described, including records of the extant P.

Chromosomal Number
The

Phylogenetic History of the Podocarpaceae
Molecular studies suggest Araucariaceae as the sister family of Podocarpaceae, although these families are morpho-anatomically divergent [4,[11][12][13], which was also supported by our results. Previous molecular and fossil records suggest that podocarps originated in the Triassic-Jurassic in Gondwana [12,85], or the Early Cretaceous [10], or Late Triassic [13], but recent podocarp fossils from Jordan push back the origin of the Podocarpaceae to the Permian (Figure 1) and show that they survived the "great dying" at the end of Permian [86,87]. Our results suggest that Lepidothamnus and Phyllocladus diverged in the Late Jurassic, when incorporating the oldest Lepidothamnus fossil record [51,88], which is earlier than the previous estimate of mid-Cretaceous-early Paleogene [10,12] and Early Jurassic [13]. Our studies recognized the presence of three major Prumnopityoid, Dacrydioid and Podocarpoid clades and a paraphyletic group similar to Chen et al. [13].
Several studies based on both morphological [7,[89][90][91][92] and molecular [7,[92][93][94][95][96] studies have been published evaluating the phylogenetic relationship among different genera of the Podocarpaceae. Based on morphology and 18S rDNA, Kelch [7] concluded that the Podocarpaceae are monophyletic except for Podocarpus (paraphyletic) and Dacrydium (polyphyletic). Conran et al. [93], based on molecular analysis (plastid rbcL), reported that Podocarpaceae are polyphyletic and supported the separation of Afrocarpus from Podocarpus and its placement as sister to Retrophyllum instead of Nageia, and also suggested that Podocarpus is monophyletic, a conclusion supported by Sinclair et al. [94]. Biffin et al. [85], based on their molecular studies of 94 Podocarpaceae species, reported that Podocarpus is closely related to Nageia, Afrocarpus and Retrophyllum. Knopf et al. [92] investigated the phylogeny of 145 species (including 77 species of Podocarpus) of Podocarpaceae based on morphological, anatomical and DNA sequences (rbcL, nrITS1 and NEEDLY). Their most significant findings were the support of subgenera in Podocarpus, the transfer of Sundacarpus amarus to Prumnopitys and the incorporation of the Phyllocladaceae into the Podocarpaceae as Phyllocladus. Lu et al. [11] reported two monophyletic sister groups: the Dacrydioid group (Dacrycarpus, Dacrydium and Falcatifolium) and the Podocarpoid group (Retrophyllum-Nageia subclade and the Afrocarpus-Podocarpus subclade). Little et al. [95] used DNA barcoding (matK, rbcL and nrITS2 DNA barcodes) for the identification of Podocarpaceae (18 genera and 145 species) and to construct a phylogenetic tree. Quiroga et al. [97], based on molecular and fossil data, reported that Podocarpus originated in late Cretaceous-early Paleogene (~63 Ma) and supported the two subgenera in Podocarpus. Leslie et al. [96], using more comprehensive sampling and markers, recognized 19 genera and supported the division of Podocarpus into two subgenera. Recently, Page [75] again split the genus Prumnopitys into three genera (Prumnopitys, Sundacarpus and the new genus Pectinopitys) based on morphological and molecular data. The current phylogeny supports the division of the 20 genera of podocarps into main three clades and a paraphyletic grade (Figure 1). Similarly, the current phylogeny also recognizes and supports the division of Podocarpus into two subgenera, i.e., Podocarpus and Foliolatus [12,13,92,97].

Historical Taxonomic Treatment
The most extensive taxonomic studies on the Podocarpaceae have been by de Laubenfels, Buchholz, Gray and Page, with many other contributions, which are summarized in Table 3. Initially, podocarps were placed in two genera, Podocarpus and Dacrydium, mainly based on leaf morphology [98]. Several early taxonomists including Gordon [111] and Philippi [112] recognized variation in Podocarpus and Dacrydium and classified them into several sections, subgenera, and subgroups. From the 1960s onwards, Podocarpus was then divided into eight genera and Dacrydium into five. Based on leaf morphology and anatomy, Podocarpus was initially divided into eight sections (Afrocarpus, Dacrycarpus, Eupodocarpus, Microcarpus, Nageia, Polypodiopsis, Stachycarpus and Sundacarpus). After a more detailed examination, de Laubenfels [113] raised section Dacrycarpus to the genus Dacrycarpus. Quinn [114] suggested raising the eight sections of Podocarpus to generic level and de Laubenfels [115] raised the section Microcarpus to generic level as Parasitaxus.

Current Diversity and Distribution of Podocarpaceae
Podocarps occur mainly in the Southern Hemisphere, although some genera extend northward, i.e., subtropical China and Japan and to Mexico and the Caribbean [125]. The living species of Podocarpaceae are a small representation of a once highly diverse group [55,126]. Today, several genera have low species representation (e.g., monospecific in Manoao, Lagarostrobos, Microcachrys, Parasitaxus and Saxegothaea and two in Acmopyle and Pherosphaera), although the fossil record suggests a more extensive diversity for at least some of these genera in the past. The center of diversity for the Podocarpaceae is Australasia (New Caledonia, Tasmania, New Zealand and Malesia), South America (Andes mountains), Indo-China and the Philippines [125,127].
Podocarps favor mostly cool and wet climates but usually do not tolerate extreme cold like some Northern Hemisphere conifers [128]. However, some temperate Podocarpaceae species occur as shrubs and prostrate woody plants above the tree line in the alpine ecosystems of Tasmania, Victoria, and New Zealand (Figure 4).
The tropical podocarps are mostly confined to mountain forests and heathlands and nutrient-poor habitats in the lowlands, although some also grow in forest understories. Temperate podocarps are good competitors in nutrient-poor soils probably because the light is more easily available within the incomplete canopies, but they are outcompeted in nutrient-rich soil as the canopy and forest floor is occupied by angiosperms and the growth of new individuals is slow due to shading. Such conditions favor broad-leaved podocarps (Nageia and broad-leaved Podocarpus species are shade-tolerant) and exclude imbricate-leaved podocarps due to competition [128]. This is supported by Adie and Lawes [129], who concluded that African podocarps are not lowland rainforest survivors but are temperate forest relicts.

Historical Biogeography
The historical reconstruction of Podocarpaceae confirms that it is a Southern Hemisphere family that was initially centered in Gondwana [130]. Leslie et al. [12] suggest that Podocarpaceae diversified in the Cretaceous and earliest Cenozoic after its appearance in the Triassic of Gondwana. Klaus and Matzke [10], based on the reconstruction of ancestral ranges, suggested that podocarps originated in the Early Jurassic in what is today Central-South America, Australia, and New Zealand. The family subsequently dominated Australasia and Southern America and later (and through to the present) in Malesia [77]. However, the discovery of macrofossils of podocarps from the early Permian of Jordan [86,87] will require a re-assessment of the early history of the family [88]. The tropical podocarps are mostly confined to mountain forests and heathlands and nutrient-poor habitats in the lowlands, although some also grow in forest understories. Temperate podocarps are good competitors in nutrient-poor soils probably because the Klaus and Matzke [10] used living taxa to reconstruct the ancestral ranges and suggested that the ancestral area for the Podocarpoid clade is the Australia-New Guinea-Malesian region; for the Dacrydioid clade it is New Caledonia; for the Prumnopityoid clade it is New Zealand and for the paraphyletic group/grade, South America to Australia. Macrofossil evidence and the historical biogeographic reconstruction by Klaus and Matzke [10] support an Australian origin of Podocarpus and multiple dispersals to South America, Asia, New Zealand, Malesia, and New Caledonia. Morley [77] concluded that Podocarpus dispersed into South Asia in the Late Eocene, either by dispersal from India or by multiple long-distance dispersal events from Australia. Similarly, he concluded that Podocarpus was possibly present in Africa during the mid-Cenozoic but its dispersal to West Africa occurred by island-hopping in the late Pliocene. According to Nieto-Blázquez et al. [131], Podocarpus species in the Caribbean are the result of colonization from the Andes during the Eocene to Oligocene (c. . Fossil records and living species distributions of Nageia support an Asian origin [10,54]. The living species of Afrocarpus strongly support an African origin for that genus. The living taxa and fossil record suggest a Gondwanan origin of Retrophyllum, with it evolving by the early Eocene [65,74]. Although the historical biogeographic reconstruction produced by Klaus and Matzke [10] suggests the origin of Dacrydium in New Caledonia, the macrofossil record strongly suggests an Australasian origin [32,39]. Morley [77] also concluded that Dacrydium originated in Australasia in the Late Cretaceous and dispersed to Southeast Asia in the Early Oligocene, probably by island-hopping (e.g., it dispersed to the Ninety East Ridge by the Paleocene and to India by the Early Eocene and later expanded to Japan during the Middle Miocene climatic optimum). According to Wu et al. [36,76], Dacrycarpus also had an Australasian origin during the Late Cretaceous. Dacrycarpus was present by the Eocene in Patagonia, supporting biogeographic connections during the warm Eocene from Patagonia to Australasia across Antarctica [35]. According to Morley [77], Dacrycarpus dispersed to New Guinea from Australia by the late Miocene and then during the mid-Pliocene, it island-hopped to Borneo, and during the Pleistocene, to Sumatra and the Malay Peninsula. However, the Dacrycarpus megafossil from the Miocene of South China shows its earlier arrival to Asia from the Southern Hemisphere and China during Late Miocene [36]. Paleoclimatic studies also support the existence of Dacrycarpus in high-precipitation areas and explain its possible extinction in Australia as that continent dried [36,85]. Dacrycarpus possibly became extinct around the Paleogene-Neogene transition from both South America and Antarctica and during the Neogene from Australia [36]. Klaus and Matzke's [10] historical biogeographic reconstruction suggests that Falcatifolium originated in the Fiji-New Guinea region around the Late Eocene. However, the fossil record of Falcatifolium from the Middle Eocene of Australia suggests an Australian origin [49], Falcatifolium probably dispersed later to New Caledonia and Papua New Guinea [84].
Klaus and Matzke [10] also concluded that the Prumnopityoid clade originated in New Zealand around the mid-Cretaceous. However, a recent phylogeny of the podocarps suggests an Early to Mid-Jurassic origin for this clade (Figure 1). Leslie et al. [5] and Wang and Ran [84] reported that the phylogenetic divergence of Podocarpaceae shows that the three genera (Lepidothamnus, Podocarpus and Prumnopitys) were dispersed from Australia to South America through Antarctica. A Lepidothamnus macrofossil from the middle Cretaceous of Winton, Queensland [51,88] also supports its Australian origin. The living and macrofossil records of Phyllocladus indicates a Gondwanan origin and wider distribution. Phyllocladus dispersed to New Guinea by the late Miocene and then, during the mid-Pliocene, it island-hopped to Borneo [77]. The extant and extinct species (Halocarpus highstedii from the Oligocene-Miocene) are endemic to New Zealand [39]. Today, Manoao is a monotypic endemic genus to New Zealand but one fossil specimen from the Oligocene (35 Ma) of Cethana, Tasmania (Australia) is similar to that of Manoao colensoi (reported as Lagarostrobos colensoi), showing this genus was once present in Australia [38]. Parasitaxus is a monotypic endemic genus to New Caledonia with no macrofossil records. Lagarostrobos is also a monotypic endemic genus in Tasmania and the macrofossil records from Early Oligocene to Early Pleistocene are also restricted to Tasmania [33,34].
Prumnopitys has three living species distributed in New Zealand and South America. The macrofossil records (Cretaceous-Miocene) demonstrate a Gondwanan origin and wider distribution [43,75]. Although Sundacarpus is now a monotypic genus, the macrofossil records (S. anglica from England and S. tzagajanicus from Russia) from the Uppermost Cretaceous and Eocene show a wider past distribution [75]. Pectinopitys is widely distributed in New Zealand, Australia, New Caledonia, and South America, but with no macrofossil record.
Klaus and Matzke [10] conclude that Acmopyle originated in New Caledonia, but macrofossils from the Eocene-Oligocene suggest a Gondwanan origin [27][28][29][30][31][32]. Microcachrys is now endemic to Australia but is also present in the Oligocene-Miocene of New Zealand [52]. Saxegothaea is the oldest genus in the family and is part of an ancient lineage endemic to South America. Pherosphaera has two living species and two macrofossils from Australia [33].

Eco-Physiological Adaptations
Most podocarps have evolved flattened leaves and fleshy seed cones, which enable them to survive in low-light conditions beneath the tree canopy and disperse their seeds biotically [85,88,132,133]. Podocarps mature as trees or shrubs. Some of the most significant ecophysiological adaptations and strategies are discussed here.

Seed Cone Morpho-Anatomy
The Podocarpaceae have evolved distinct seed cone morphotypes and display marked variation in functional traits across the 20 genera [88,133,134]. Most podocarp genera produce fleshy seed cones utilizing the epimatium, aril, bracts, receptaculum or a combination of these [109]. Podocarpus is the largest genus in the Podocarpaceae and has a cone composed of one or two seeds covered mostly by a papery and sometimes a fleshy epimatium [10,109]. Several podocarp genera have cones with a brightly colored, fleshy receptaculum [10,88,134].

Leaf Morpho-Anatomy
The Podocarpaceae is prominent in many mixed conifer/broadleaf vegetation types in the Southern Hemisphere, and they exhibit great variation in leaf morphology across the 20 genera [135]. The diversity in leaf morphology of Podocarpaceae is remarkable, ranging from uni-veined needle and scale-like leaves to multi-veined broad leaves. Podocarpaceae foliage can be divided into two main types, imbricate (Dacrycarpus, Dacrydium, Halocarpus, Manoao, Lagarostrobos, Lepidothamnus, Microcachrys, Pherosphaera and Parasitaxus) and broad (flattened) leaved (Acmopyle, Nageia, Afrocarpus, Falcatifolium, Phyllocladus, Podocarpus, Retrophyllum, Pectinopitys, Sundacarpus, Prumnopitys and Saxegothaea). These genera have leaves either spirally arranged or in opposite pairs. Most Podocarpaceae species possess flattened or composite leaves (in 11 genera and more than 140 species) and this may be an adaptation to light requirements, as most of these species grow in the understory of forests with a low-light environment and are unable to reach the canopy level and high sunlight [9] unless a canopy gap occurs. Nageia is characterized by having leaves with multiple parallel veins [55]. All Phyllocladus species have evolved multi-veined phylloclades (Supplementary Figure S1), probably to compete with angiosperms for light [9,82,136]. Acmopyle, Dacrycarpus and Falcatifolium have bilaterally flattened leaves, lacking a true petiole. Leaf dimorphism is present in many genera of Podocarpaceae (Supplementary Figure S2). All other broad-leaved species have bifacially flattened broad leaves [135].

Pollen Morphology
All conifer species are wind-pollinated and those in the Podocarpaceae (except Saxegothaea) and Pinaceae have developed special wing-like structures called sacci [2]. The Podocarpaceae usually have saccate pollen with a tectate exine but usually with a smaller grain than the Pinaceae [137]. Pollen of all genera are bi-saccate except Microcachrys, Pherosphaera and Dacrycarpus, which are tri-saccate, and Saxegothaea which does not have sacci [91,138,139]. Because of this, Erdtman [138] suggested shifting Saxegothaea to the Araucariaceae, while Gaussen [103] and Woltz [140] suggested promoting it to the new family Saxegothaeaceae. The fossil pollen record of the Podocarpaceae is not considered here but is in need of revision, with much important data currently difficult to assess without expert comment on the validity of published interpretations.
Leslie et al. [96] reported that cone morphology and seed size are co-evolved in a correlated pattern in animal-dispersed conifers and animal-dispersed species have a relatively larger seed size to attract animals. Similarly, climate change (higher temperatures or water stress in drier conditions) can affect the evolution of cone shape. Interpreting the cone morphology and animal dispersal in Podocarpaceae is difficult because animal-dispersed seeds (fleshy cones) evolved many times in the deep past (from the Cretaceous or even earlier, based on ancestral reconstruction) [88,96,134]. Podocarpus can be interpreted as zoochorous and mainly bird-dispersed due to their colorful fleshy receptacle and epimatium. Bird and bat dispersal have been reported from South African podocarps [142]. The Emu (Dromaius novaehollandiae) is a large bird with a wide distribution range in Australia and it is the main disperser of Podocarpus drouynianus in southwestern Australia, keeping the seeds for up to 50 h in the digestive tract and dispersing them several kilometers [143].

Ecology of Podocarpaceae
The major Southern Hemisphere conifer family Podocarpaceae is different in morphology, functional physiology, and ecology from the Northern Hemisphere's major conifer family Pinaceae. Pinaceae are successful in Northern Hemisphere forests, where angiosperms are outcompeted during freezing temperatures, and also occur in low-rainfall areas. Podocarp species are more abundant and compete more successfully with broadleaf angiosperms in the tropical montane forest through multiple morphological and anatomical adaptations but in most cases avoid low-rainfall areas [144]. Ecologically, podocarps have a highly conserved association with the conifer families Araucariaceae and Cupressaceae and with the angiosperm families Nothofagaceae, Winteraceae and Cunoniaceae [9,136]. However, ecological data are lacking for most of the species in these families [4].
Podocarps are unable to bear extreme cold temperate but can tolerate moderate frosts [128] and some exist as alpine shrubs in relatively cold climates (e.g., alpine Tasmania) where permanent snow is uncommon (Figure 4). They possess broad to scale leaves, phylloclades and fleshy cones and they are adapted to a range of conditions from alpine to lowland, understory environments beneath a dense canopy, semi-aquatic (Retrophyllum minus), drought-and fire-prone conditions (Podocarpus drouynianus). The only parasitic gymnosperm (Parasitaxus usta) grows on the roots of another podocarp species (Falcatifolium taxoides). The occurrence of extant species of Podocarpaceae in angiosperm-dominated humid forests is of great interest to ecologists and paleontologists. The Podocarpaceae have preferred wet climates throughout their history [77] and nutrients are a stronger limiting factor for their distribution than the temperature [145], with Coomes and Bellingham [128] reporting that within temperate and tropical rainforests with few exceptions, podocarps are well adapted to nutrient-poor soils.
Coomes and Bellingham [128] evaluated the ecological similarities and differences of temperate and tropical podocarps. They concluded that angiosperm diversification and expansion during the Late Cretaceous was responsible for driving conifers from the lowland tropics and mesic temperate regions due to inferior reproductive competitiveness. However, Bond [146] and Midgley and Bond [147] challenged this view and hypothesized that the physiological traits of conifers (slow seedling establishment and later growth) put them at a disadvantage in competitive regeneration in changing climates (increasing cold and droughts) and habitats (nutrient-poor soil, poorly drained soil, and low light). Podocarps are predominantly slow-growing with low photosynthetic capacity per unit leaf mass and per unit leaf area compared with angiosperms with the same leaf are [128]. The studies that evaluated the growth of podocarps in different habitats lead to the conclusion that podocarp growth is slow compared to other conifers and to angiosperms (e.g., in lowland cool temperate forest, the growth rate is half that of angiosperms [148], and in subalpine shrublands, podocarps grow more slowly than several angiosperm species [149]. In the nutrient-rich soil of southern New Zealand, even tree ferns grow faster than podocarps [150,151]. Brodribb [144] argues that drought is one of the major agents that prevents podocarp success at high altitudes in the Southern Hemisphere. The Late Cenozoic was a major drying period in the temperate region and resulted in the contraction and extinction of Australian and other southern podocarps [152]. The cool and wet conditions (on the continental margins of Gondwana) necessary for the diversification of the Podocarpaceae favor the theory of the drought sensitivity of Podocarps [135,153]. High wood density (that lowers hydraulic efficiency) and leaf sclereids (that collapse under water tension, which results in a loss of hydraulic and photosynthetic function in the leaf) are also present in the broad-leaved tropical podocarps and may be the cause of poorer drought performance and weak competition in drier forests but favor cool, shady, and wet regions of the Southern Hemisphere for podocarp persistence [135,144,154]. In contrast, the Pinaceae have tough and waxy needle-like leaves, lower wood density, fewer sclereids and a high photosynthetic rate, making them resistant and adaptable to drought and freezing temperatures that are common in parts of the Northern Hemisphere [144,155]. This also provides a possible insight into why podocarps are today almost absent from the Northern Hemisphere, despite their potential for long-distance dispersal. A few podocarps are tolerant of drier regions, e.g., Afrocarpus falcatus (southern Africa), Podocarpus drouynianus (Western Australia) and Halocarpus bidwillii, Phyllocladus alpinus and Podocarpus laetus (dry lowland forests of New Zealand) [134]. Podocarp morphology is unusual compared to other conifers, since, despite possessing thick tracheid walls that are vulnerable to embolism at low tensions [154]. (Pittermann et al., 2006b), they also have high hydraulic resistance across pit membranes [156] and that makes the implosion of sclereids in podocarp leaves under tension a real possibility [157].
(CR) species are Acmopyle sahniana (Fiji), Pherosphaera fitzgeraldii (Australia), Dacryd guillauminii (New Caledonia), Podocarpus urbanii (Jamaica), P. costaricensis (Costa Rica Panama), P. decumbens (New Caledonia), P. palawanensis (the Philippines), P. perrieri (M agascar) and P. sellowii var. angustifolius (Brazil). The IUCN conservation status for tr cal podocarps states that 5 species are considered critically endangered, 18 species endangered, and 16 species are vulnerable . The New Caledo podocarp species are facing serious conservation threats due to their restricted pop tions (Enright and Jaffré, 2011); i.e., Retrophyllum minus (endangered), Podocarpus dec bens (critically endangered) P. longefolaliatus (endangered), Dacrydium guillauminii (c cally endangered), Acmopyle pancheri (nearly threatened) and Parasitaxus usta (vulnera Deforestation associated with mining, expansion of tropical agricultural activ and other anthropogenic activities poses a serious threat to tropical podocarps [158]. forestation and climate change are also posing a serious threat to montane endemic p carps [159]. Similarly, more extreme dry seasons are also damaging for tropical podoc because they are drought and fire intolerant [158]. Wildfire is posing a huge threat to A tralian podocarps ( Figure 6) and in some areas, the podocarp population has been dr to extinction by these fires [160]. The harvest of podocarp timber has been an impor industry, but their slow growth makes it detrimental and unsustainable for the spe involved [161]. Mill [162] reported habitat loss, climate change and deforestation as m Deforestation associated with mining, expansion of tropical agricultural activities and other anthropogenic activities poses a serious threat to tropical podocarps [158]. Deforestation and climate change are also posing a serious threat to montane endemic podocarps [159]. Similarly, more extreme dry seasons are also damaging for tropical podocarps because they are drought and fire intolerant [158]. Wildfire is posing a huge threat to Australian podocarps ( Figure 6) and in some areas, the podocarp population has been driven to extinction by these fires [160]. The harvest of podocarp timber has been an important industry, but their slow growth makes it detrimental and unsustainable for the species involved [161]. Mill [162] reported habitat loss, climate change and deforestation as major threats causing the extinction of Podocarpus species. Failure of regeneration and aging of the current populations are two major threats for at least some podocarp species [128,163,164].
Plants 2023, 12, x FOR PEER REVIEW 38 o threats causing the extinction of Podocarpus species. Failure of regeneration and aging the current populations are two major threats for at least some podocarp spec [128,163,164]. Figure 6. A wildfire in 2020 burnt the Tahune rainforest, Tasmania. This photo is of a burnt Cele top Pine (Phyllocladus aspleniifolius) tree. Figure 6. A wildfire in 2020 burnt the Tahune rainforest, Tasmania. This photo is of a burnt Celery-top Pine (Phyllocladus aspleniifolius) tree.

Current Gaps and Future Perspectives
Some clear gaps still exist that need to be filled in order for us to gain a better understanding of the Podocarpaceae and include some of the following aspects: 1.
Descriptions and taxonomic treatments of several species from less explored/remote areas such as Papua New Guinea, Malaysia, Indonesia, and New Caledonia are based only on collections of one or a few specimens. Additionally, some of these areas are not well explored and may contain undescribed species.

2.
Field-and laboratory-based studies on pollination biology, the reproductive cycle and anatomical structures are not well developed for most podocarps and require further detailed evaluation.

3.
Extensive research is required to understand why Podocarpaceae have such remarkable seed cone and leaf morphology.

4.
Very few studies report the dispersal biology of podocarp seeds and comprehensive assessments are required to understand the dispersal biology and ecology of podocarps.

5.
Despite the several high-quality publications on the leaf cuticle morphology of various genera, a good quality publication is necessary that describes the taxonomic and phylogenetic authenticity of these foliar cuticular diagnostic characters. Similarly, studies are required to assess the infraspecific variation in the leaf morphology for different populations. 6.
Phylogenomic and population-based studies are available only for a few Podocarpus species (P. matudae, P. nubigenus, P. parlatorei, P. salignus, P. latifolius, P. guatemalensis and P. oleifolius), and with fairly limited geographic scope (the Americas). With the availability of modern NGS techniques and bioinformatic tools, more comprehensive studies are required to unveil their phylogeny, historical biogeography, speciation, and population history. 7.
Only a few studies are available on the historical biogeography of Podocarpaceae and the discovery of new podocarp fossils from the Early Permian (Paleozoic) of Jordan [86,87] questions the Gondwanan origin of the Podocarpaceae. The inclusion of well-placed podocarp fossils will help in better understanding the reconstruction of historical biogeography. 8.
Comparative studies of the three Southern Hemisphere conifer families (Araucariaceae, Cupressaceae and Podocarpaceae) to evaluate the impact of these families on the habitats they occupy and their relationships with the rest of the Southern Hemisphere biota. 9.
Evolution of photosynthetic units in these three families in response to the closed forests that predated the rise to dominance of the angiosperms and angiospermdominated rainforests and then the major aridification of the Southern Hemisphere. 10. A better understanding of the response of podocarp foliage to drought stress and the adaptations that have evolved to deal with the constraint of most podocarps in having only a single vein per leaf is required to better understand the distribution and ecology of the family. 11. Use of species distribution modelling to predict the possible ecological niche and the effect of climate change on species range dynamic. 12. A better understanding of the evolutionary history and biology, ecology and life history are important in conservation efforts, given that so many species are threatened.

Conclusions
The current study provides a comprehensive overview on the systematics, diversity, hotspots, evolutionary adaptations, and conservation status of podocarps. Podocarps are morphologically more diverse compared to other conifer families and the updated phylogeny based on more extensive macrofossil records broadens our understanding of the evolutionary history of Podocarpaceae. Most podocarp genera currently exhibit low species richness and high endemism and often have disjunct distributions. Today, the Malesian region is the diversity hotspot for living podocarp taxa. However, the fossil record demonstrates wider distributions in the past. Podocarpus, Dacrydium and Dacrycarpus are the most dominant genera (approximately 75% of living podocarps) and have acquired particular morpho-anatomical adaptations that help them to survive in tropical forests. Podocarps demonstrate a remarkable seed cone and leaf diversity compared with other conifers. The genera with fleshy seed cones predominantly rely on bird dispersal. Podocarps are facing serious threats from deforestation, climate change, drought and wildfire, and the need for further targeted research is urgent. Among the conifers, podocarps are less well known and receive less attention than their counterparts that dominate the Northern Hemisphere, despite their remarkable morphological diversity and long evolutionary history.